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J Neurophysiol 102: 2039-2054, 2009. First published July 22, 2009; doi:10.1152/jn.00075.2009
0022-3077/09 $8.00

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RESEARCH-ARTICLE

Encoding and Decoding of Learned Smooth-Pursuit Eye Movements in the Floccular Complex of the Monkey Cerebellum

¹Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania; and ²Howard Hughes Medical Institute, W. M. Keck Foundation Center for Integrative Neuroscience, and Department of Physiology, University of California, San Francisco, San Francisco, California

Submitted 23 January 2009; accepted in final form 21 July 2009

ABSTRACT

We recorded the simple-spike (SS) firing of Purkinje cells (PCs) in the floccular complex both during normal pursuit caused by step-ramp target motions and after learning induced by a consistently timed change in the direction of target motion. The encoding of eye movement by the SS firing rate of individual PCs was described by a linear regression model, in which the firing rate is a sum of weighted components related to eye acceleration, velocity, and position. Although the model fit the data well for individual conditions, the regression coefficients for the learned component of firing often differed substantially from those for normal pursuit of step-ramp target motion. We suggest that the different encoding of learned versus normal pursuit responses in individual PCs reflects different amounts of learning in their inputs. The decoded output from the floccular complex, estimated by averaging responses across the population of PCs, also was fitted by the regression model. Regression coefficients were equal for the two conditions for on-direction pursuit, but differed for off-direction target motion. We conclude that the average output from the population of floccular PCs provides some, but not all, of the neural signals that drive the learned component of pursuit and that plasticity outside of the flocculus makes an important contribution.